Development of chloride-mediated inhibition in neurons of the anteroventral cochlear nucleus of gerbil (Meriones unguiculatus)

Journal of Neurophysiology

Volumn 98, Issue 3, 2007, Pages 1634-1644

  Milenković, Ivan ^a   Witte, Mirko ^a   Tureček, Rostislav ^b   Heinrich, Marco ^a   Reinert, Thomas ^a   Rübsamen, Rudolf ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b INSTITUTE OF MATHEMATICS   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ALKANOIC ACID; CHLORIDE; COTRANSPORTER; FUROSEMIDE; GRAMICIDIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COCHLEAR NUCLEUS; CONTROLLED STUDY; DEPOLARIZATION; EVOKED RESPONSE; GABAERGIC TRANSMISSION; GERBIL; HYPERPOLARIZATION; MERIONES UNGUICULATUS; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL;

ANIMALS; BRAIN STEM; CHLORIDES; COCHLEAR NUCLEUS; ELECTROPHYSIOLOGY; FUROSEMIDE; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GERBILLINAE; GLYCINE; MUSCIMOL; NEURONS; PYRIDAZINES; RECEPTORS, GABA-A; SYNAPTIC TRANSMISSION;

EID: 34548792310     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01150.2006     Document Type: Article

References (106)

1. Altschuler RA, Juiz JM, Shore SE, Bledsoe SC, Helfert RH, Wenthold RJ. Inhibitory amino acid synapses and pathways in the ventral cochlear nucleus. In: The Mammalian Cochlear Nuclei: Organization and Function, edited by Merchan MA. New York: Plenum, 1993, p. 211-224.
2. Akaike N. Gramicidin perforated patch recording and intracellular chloride activity in excitable cells. Prog Biophys Mol Biol 65: 251-264, 1996.
3. Backoff PM, Palombi PS, Caspary DM. Glycinergic and GABAergic inputs affect short-term suppression in the cochlear nucleus. Hear Res 110: 155-163, 1997.
4. Backoff PM, Shadduck Palombi P, Caspary DM. Gamma-aminobutyric acidergic and glycinergic inputs shape coding of amplitude modulation in the chinchilla cochlear nucleus. Hear Res 134: 77-88, 1999.
5. Balakrishnan V, Becker M, Löhrke S, Nothwang HG, Güresis E, Friauf E. Expression and function of chloride transporters during development of inhibitory neurotransmission in the auditory brain stem. J Neurosci 23: 4134-4145, 2003.
6. Baumann SW, Baur L, Siegel E. Individual properties of the two functional agonist sites in GABA(A) receptors. J Neurosci 23: 11158-11166, 2003.
7. Bazwinsky I, Rübsamen R. Development of expression of calcium binding proteins in auditory brain stem nuclei. In: Abstracts of the Twenty-Third Midwinter Research Meeting, edited by Popelka GR. St. Peterburg Beach, FL: Assoc. Res. Otolaryngol., 2000, vol. 23, p. 2460.
8. Ben-Ari Y. Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3: 728-739, 2002.
9. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL. Giant synaptic potentials in immature rat CA3 hippocampal neurons. J Physiol 416: 303-325, 1989.
10. Benson CG, Potashner SJ. Retrograde transport of [3H]glycine from the cochlear nucleus to the superior olive in the guinea pig. J Comp Neurol 296: 415-426, 1990.
11. Blaesse P, Guillemin I, Schindler J, Schweizer M, Delpire E, Khiroug L, Friauf E, Nothwang HG. Oligomerization of KCC2 correlates with development of inhibitory neurotransmission. J Neurosci 26: 10407-10419, 2006.
12. Bormann J, Hamill OP, Sakmann B. Mechanism of anion permeation through channels gated by glycine and γ-amino-butiryc acid in mouse cultured spinal neurons. J Physiol 385: 243-286, 1987.
13. Brawer JR, Morest DK. Relations between auditory nerve endings and cell types in the cat's anteroventral cochlear nucleus seen with the Golgi method and Nomarski optics. J Comp Neurol 160: 491-506, 1975.
14. Carr CE, Fujita I, Konishi M. Distribution of GABAergic neurons and terminals in the auditory system of the barn owl. J Comp Neurol 286: 190-207, 1989.
15. Caspary DM, Backoff PM, Finlayson PG, Palombi PS. Inhibitory inputs modulate discharge rate within frequency receptive fields of anteroventral cochlear nucleus neurons. J Neurophysiol 72: 2124-2133, 1994.
16. Cherubini E, Rovira C, Gaiarsa JL, Corradetti R, Ben-Ari Y. GABA mediated excitation in immature CA3 hippocampal neurons. Int J Dev Neurosci 8: 481-490, 1990.
17. Chery N, de Koninck Y. Junctional versus extrajunctional glycine and GABA(A) receptor-mediated IPSCs in identified lamina I neurons of the adult rat spinal cord. J Neurosci 19: 7342-7355, 1999.
18. Chudotvorova I, Ivanov A, Rama S, Hübner CA, Pellegrino C, Ben-Ari Y, Medina I. Early expression of KCC2 in rat hippocampal cultures augments expression of functional GABA synapses. J Physiol 566: 671-679, 2005.
19. Code RA, Rubel EW. Glycine-immunoreactivity in the auditory brain stem of the chick. Hear Res 40: 167-172, 1989.
20. Cordero-Erausquin M, Coul JA, Boudreau D, Rolland M, De Koninck Y. Differential maturation of GABA action and anion reversal potential in spinal lamina I neurons: impact of chloride extrusion capacity. J Neurosci 25: 9613-9623, 2005.
21. Coull JA, Boudreau D, Bachand K, Prescott SA, Nault F, Sik A, De Koninck P, De Koninck Y. Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 424: 938-942, 2003.
22. - regulation. J Physiol 520: 121-137, 1999.
23. 2+ signalling in developing rat cerebellar Purkinje neurons. J Physiol 536: 429-437, 2001.
24. Funabiki K, Koyano K, Ohmori H. The role of GABAergic inputs for coincidence detection in the neurons of nucleus laminaris of the chick. J Physiol 508: 851-869, 1998.
25. Ganguly K, Schneider AF, Wong ST, Poo M. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105: 521-532, 2001.
26. -]-cotransporter system. Mol Pharmacol 33: 696-701, 1988.
27. Grothe B. New roles for synaptic inhibition in sound localization. Nat Rev Neurosci 4: 540-550, 2003.
28. Gulyas AJ, Sik A, Payne JA, Kaila K, Freund TF. The KCl cotransporter, KCC2, is highly expressed in the vicinity of excitatory synapses in the rat hippocampus. Eur J Neurosci 13: 2205-2217, 2001.
29. Härtig W, Singer A, Grosche J, Brauer K, Ottersen OP, Bruckner G. Perineuronal nets in the rat medial nucleus of the trapezoid body surround neurons immunoreactive for various amino acids, calcium-binding proteins and the potassium channel subunit Kv3.1b. Brain Res 899: 123-133, 2001.
30. Hyson RL, Reyes AD, Rubel EW. A depolarizing inhibitory response to GABA in brain stem auditory neurons of the chick. Brain Res 677: 117-126, 1995.
31. i in retinal neurons of postnatal rabbits. Vis Neurosci 13: 441-447, 1996.
32. - accumulation and depletion in cultured rat midbrain neurons. J Neurosci 19: 4695-4704, 1999.
33. A receptor. J Neurosci 18: 8590-8604, 1998.
34. B binding sites in the cochlear nucleus of the guinea pig. Brain Res 639: 193-201, 1994.
35. Juiz JM, Helfert RH, Bonneau JM, Wenthold RJ, Altschuler RA. Three classes of inhibitory amino acid terminals in the cochlear nucleus of the guinea pig. J Comp Neurol 73: 11-26, 1996.
36. Juiz JM, Helfert RH, Wenthold RJ, De Blas AL, Altschuler RA. Immunocytochemical localization of the GABAA/benzodiazepine receptor in the guinea pig cochlear nucleus: evidence for receptor localization heterogeneity. Brain Res 504: 173-179, 1989.
37. A receptor channel function in the nervous system. Prog Neurobiol 42: 489-537, 1994.
38. + transient. J Neurosci 17: 7662-7672, 1997.
39. Kakazu Y, Norio A, Komiyama S, Nabekura J. Regulation of intracellular chloride by cotransporters in developing lateral superior olive neurons. J Neurosci 19: 2843-2851, 1999.
40. - cotransport in rat central neurons. J Neurophysiol 84: 281-288, 2000.
41. Kanaka C, Ohno K, Okabe A, Kuriyama K, Itoh T, Fukuda A, Sato K. The differential expression patterns of messenger RNAs encoding K-Cl cotransporters (KCC 1,2) and Na-K-2Cl cotransporter (NKCC1) in the rat nervous system. Neuroscience 104: 933-946, 2001.
42. Kandler K, Friauf E. Development of glycinergic and glutamatergic synaptic transmission in the auditory brain stem of perinatal rats. J Neurosci 15: 6890-6904, 1995.
43. Kelsch W, Hormuzdi S, Straube E, Lewen A, Monyer H, Misgeld U. Insulin-like growth factor 1 and a cytosolic tyrosine kinase activate chloride outward transport during maturation of hippocampal neurons. J Neurosci 21: 8339-8347, 2001.
44. Khirug S, Huttu K, Ludwig A, Smirnov S, Voipio J, Rivera C, Kaila K, Khiroug L. Distinct properties of functional KCC2 expression in immature mouse hippocampal neurons in culture and in acute slices. Eur J Neurosci 21: 899-904, 2005.
45. Kocsis JD, Rand MN, Lankford KL, Waxman SG. Intracellular calcium mobilization and neurite outgrowth in mammalian neurons. J Neurobiol 25: 252-264, 1993.
46. Kopp-Scheinpflug K, Dehmel S, Dörrscheidt J, Rübsamen R. Interaction of excitation and inhibition in anteroventral cochlear nucleus neurons that receive large endbulb synaptic endings. J Neurosci 22: 11104-11118, 2002.
47. Kyrozis A, Reichling DB. Perforated-patch recording with gramicidin avoids artifactual changes in intracellular chloride concentration. J Neurosci 57: 27-35, 1995.
48. Lachica EA, Rubsamen R, Rubel EW. GABAergic terminals in nucleus magnocellularis and laminaris originate from the superior olivary nucleus. J Comp Neurol 348: 403-418, 1994.
49. Lauder JM. Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Trends Neurosci 16: 233-240, 1993.
50. Lim R, Alvarez FJ, Walmsley B. Quantal size is correlated with receptor cluster area at glycinergic synapses in the rat brain stem. J Physiol 516: 505-512, 1999.
51. Lim R, Alvarez FJ, Walmsley B. GABA mediates presynaptic inhibition at glycinergic synapses in a rat auditory brain stem nucleus. J Physiol 2000 525: 447-459, 2000.
52. Lim R, Oleskevich S, Few AP, Leao RN, Walmsley B. Glycinergic mIPSCs in mouse and rat brain stem auditory nuclei: modulation by ruthenium red and the role of calcium stores. J Physiol 546: 691-699, 2003.
53. Lo Turco JJ, Blanton MG, Kriegstein AR. Initial expression and endogenous activation of NMDA channels in early neocortical development. J Neurosci 11: 792-799, 1991.
54. Löhrke S, Srinivasan G, Oberhofer M, Doncheva E, Friauf E. Shift from depolarizing to hyperpolarizing glycine action occurs at different perinatal ages in superior olivary complex nuclei. Eur J Neurosci 22: 2708-2722, 2005.
55. Lu J, Karadsheh M, Delpire E. Developmental regulation of the neuronalspecific isoform of K-Cl cotransporter KCC2 in postnatal rat brains. J Neurobiol 39: 558-568, 1999.
56. Lu T, Trussell LO. Mixed excitatory and inhibitory GABA-mediated transmission in chick cochlear nucleus. J Physiol 535: 125-131, 2001.
57. Ludwig A, Hong L, Saarma M, Kaila K, Rivera C. Developmental upregulation of KCC2 in the absence of GABAergic and glutamatergic transmission. Eur J Neurosci 18: 3199-3206, 2003.
58. Luhmann HJ, Prince DA. Postnatal maturation of the GABAergic system in rat neocortex. J Neurophysiol 65: 247-263, 1991.
59. Luhmann HJ, Reiprich RA, Hanganu I, Kilb W. Cellular physiology of the neonatal rat cerebral cortex: intrinsic membrane properties, sodium and calcium currents. J Neurosci Res 62: 574-584, 2000.
60. Mahendrasingam S, Wallam CA, Polwart A, Hackney CM. An immunogold investigation of the distribution of GABA and glycine in nerve terminals on the somata of spherical bushy cells in the anteroventral cochlear nucleus of the guinea pig. Eur J Neurosci 19: 993-1004, 2004.
61. Martina M, Royer S, Pare D. Cell-type-specific GABA responses and chloride homeostasis in the cortex and amygdala. J Neurophysiol 86: 2887-2895, 2001.
62. McCormick DA, Prince DA. Post-natal development of electrophysiological properties of rat cerebral cortical pyramidal neurons. J Physiol 393: 743-762, 1987.
63. McGinley MJ, Oertel D. Rate thresholds determine the precision of temporal integration in principal cells of the ventral cochlear nucleus. Hear Res 216-217: 52-63, 2006.
64. Monsivais P, Rubel EW. Accommodation enhances depolarizing inhibition in central neurons. J Neurosci 21: 7823-7830, 2001.
65. Oberdorfer MD, Parakkal MH, Altschuler RA, Wenthold RJ. Ultrastructural localization of GABA-immunoreactive terminals in the anteroventral cochlear nucleus of the guinea pig. Hear Res 33: 229-238, 1988.
66. Oertel D. Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus. J Neurosci 3: 2043-2053, 1983.
67. Oertel D. The role of timing in the brain stem auditory nuclei of vertebrates. Annu Rev Physiol 61: 497-519, 1999.
68. Ostapoff EM, Benson CG, Saint Marie RL. GABA- and glycine-immunoreactive projections from the superior olivary complex to the cochlear nucleus in guinea pig. J Comp Neurol 381: 500-512, 1997.
69. Ostapoff EM, Morest DK, Potashner SJ. Uptake and retrograde transport of [3H]GABA from the cochlear nucleus to the superior olive in the guinea pig. J Chem Neuroanat 3: 285-295, 1990.
70. Owens DF, Boyce HL, Davis MBE, Kriegstein AR. Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J Neurosci 16: 6414-6423, 1996.
71. Owens DF, Kriegstein AR. Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 3: 715-727, 2002.
72. Payne JA, Stevenson TJ, Donaldson LF. Molecular characterization of a putative K-Cl cotransporter in rat brain. A neuronal-specific isoform. J Biol Chem 271: 16245-16252, 1996.
73. Price GD, Trussell LO. Estimate of the chloride concentration in a central glutamatergic terminal: a gramicidin perforated-patch study on the calyx of Held. J Neurosci 26: 11432-11436, 2006.
74. Reichling DB, Kyrozis A, Wang J, MacDermott AB. Mechanisms of GABA and glycine depolarization-induced calcium transients in rat dorsal horn neurons. J Physiol 476: 411-421, 1994.
75. Rivera C, Voipio J, Kaila K. Two developmental switches in GABAergic signalling: the K-Cl cotransporter KCC2, and carbonic anhydrase CAVII. J Physiol 562: 27-36, 2005.
76. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397: 251-255, 1999.
77. Rivera C, Voipio J, Thomas-Crussels J, Li H, Emri Z, Sipilä S, Payne JA, Minichielo L, Saarma M, Kaila K. Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J Neurosci 24: 4683-4691, 2004.
78. Ryugo DK, Sento S. (1991) Synaptic connections of the auditory nerve in cats: relationship between endbulbs of held and spherical bushy cells. J Comp Neurol 305: 35-48, 1991.
79. Saint Marie RL, Morest DK, Brandon CJ. The form and distribution of GABAergic synapses on the principal cell types of the ventral cochlear nucleus of the cat. Hear Res 42: 97-112, 1989.
80. Sanes DH, Friauf E. Development and influence of inhibition in the lateral superior olivary nucleus. Hear Res 147: 46-58, 2000.
81. i in newborn rat cortex. Neuroreport 13: 2433-2437, 2002.
82. Smith PH, Joris PX, Yin TC. Projections of physiologically characterized spherical bushy cell axons from the cochlear nucleus of the cat: evidence for delay lines to the medial superior olive. J Comp Neurol 331: 245-260, 1993.
83. 2+ spikes and waves in embryonic neurons: signaling systems for differentiation. Trends Neurosci 17: 115-118, 1994.
84. Staley KJ, Proctor WR. Modulation of mammalian dendritic GABA(A) receptor function by the kinetics of Cl- and HCO3- transport. J Physiol 519: 693-712, 1999.
85. A receptors. Science 269: 977-981, 1995.
86. Stein V, Hermans-Borgmeyer I, Jentsch TJ, Hübner CA. Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. J Comp Neurol 468: 57-64, 2004.
87. Takahashi T. Inhibitory miniature synaptic potentials in rat motoneurons. Proc R Soc Lond B Biol Sci 221: 103-109, 1984.
88. - in hippocampal CA3 neurons. J Neurophysiol 61: 512-523, 1989.
89. Titz S, Hans M, Kelsch W, Lewen A, Swandulla D, Misgeld U. Hyperpolarizing inhibition develops without trophic support by GABA in cultured rat midbrain neurons. J Physiol 550: 719-730, 2003.
90. Tyzio R, Ivanov A, Bernard C, Holmes GL, Ben-Ari Y, Khazipov R. Membrane potential of CA3 hippocampal pyramidal cells during postnatal development. J Neurophysiol 90: 2964-2972, 2003.
91. - cotransporter KCC2 in the cochlear nucleus. Hear Res 206: 107-115, 2005.
92. Vu TQ, Payne JR, Copenhagen DR. Localization and developmental expression patterns of the neuronal K-Cl cotransporter (KCC2) in the rat retina. J Neurosci 20: 1414-1423, 2000.
93. Wenthold RJ. Evidence for a glycinergic pathway connecting the two cochlear nuclei: an immunocytochemical and retrograde transport study. Brain Res 415: 183-187, 1987.
94. Wenthold RJ. Neurotransmitters of auditory brain stem nuclei. In: Neurobiology of Hearing: The Central Auditory System, edited by Altschuler RA, Bobbin RP, Clopton BM, Hoffman DW. New York: Raven, 1991, p. 121-139.
95. Wenthold RJ, Parakkal MH, Oberdorfer MD, Altschuler RA. Glycine receptor immunoreactivity in the ventral cochlear nucleus of the guinea pig. J Comp Neurol 276: 423-435, 1988.
96. Wickesberg RE, Oertel D. Delayed, frequency-specific inhibition in the cochlear nuclei of mice: a mechanism for monaural echo suppression. J Neurosci 10: 1762-1768, 1990.
97. Williams JR, Sharp JW, Kumari VG, Wilson M, Payne JA. The neuronspecific K-Cl cotransporter, KCC2. Antibody development and initial characterization of the protein. J Biol Chem 274: 12656-12664, 1999.
98. Woolf NK, Ryan AF. The development of auditory function in the cochlea of the mongolian gerbil. Hear Res 13: 277-283, 1984.
99. Wu SH, Oertel D. Intracellular injection with horseradish peroxidase of a physiologically characterized stellate and bushy cells in slices of mouse anteroventral cochlear nucleus. J Neurosci 6: 2691-2706, 1984.
100. Wu SH, Oertel D. Maturation of synapses and electrical properties of cells in the cochlear nuclei. Hear Res 30: 99-110, 1987.
101. Wu WL, Ziskind-Conhaim L, Sweet MA. Early development of glycine- and GABA-mediated synapses in rat spinal cord. J Neurosci 12: 3935-3945, 1992.
102. - uptake promoting depolarizing GABA actions in immature rat neocortical neurons is mediated by NKCC1. J Physiol 557: 829-841, 2004.
103. Yang L, Monsivais P, Rubel EW. The superior olivary nucleus and its influence on nucleus laminaris: a source of inhibitory feedback for coincidence detection in the avian auditory brain stem. J Neurosci 19: 2313-2325, 1999.
104. Yoshimura M, Nishi S. Primary afferent-evoked glycine- and GABA-mediated IPSPs in substantia gelatinosa neurons in the rat spinal cord in vitro. J Physiol 482: 29-38, 1995.
105. 2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 6: 333-344, 1991.
106. Zhou FM, Hablitz JJ. Postnatal development of membrane properties of layer I neurons in rat neocortex. J Neurosci 16: 1131-1139, 1996.